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Reprinted from the International Zoo Yearbook Vol. 18 1978 7 
Reproduction, growth and parental care in Crab- 
eating foxes 
Cerdocyon thous 
at the National Zoological Park, Washington 
CHARLES A. BRADY 
National Zoological Park, Smithsonian Institution, Washington, DC 200og and Department of Zoology, Ohio 
University, Athens, Ohio 45701, USA 
The Crab-eating fox Cerdocyon thous is a small 
canid with a wide distribution in South America. 
In nature, they are most often observed in pairs 
and they form long-term pair bonds in captivity 
(Kleiman & Brady, 1978). Little has been pub- 
lished on their breeding habits and captive man- 
agement (CoimbraFilho, 1966) and when, in 1975, 
the National Zoological Park's Conservation and 
Research Center initiated a long-term investi- 
gation into the breeding habits and social 
behaviour of South American canids, they were 
one of the species included. The following 
report summarises information on the repro- 
duction, behaviour and physical development of 
three pairs of captive Crab-eating foxes and their 
18 offspring during the period January 1976 to 
the end of February 1977., 
MAINTENANCE 
Each pair of foxes is housed in a 1-2 x 2-4 m 
indoor den with an adjoining 9x5m outdoor 
yard and access to a 2-5 x 36 m indoor run 
during the winter months. Pregnant $? are 
provided with a nestbox with a transparent top 
and the dens are illuminated with red light 
which permits observations, through a small hole 
in the den ceiling, of the parents and young 
without disturbing them. 
The animals are each fed 300 g of Nebraska 
Brand feline diet daily with an occasional mouse 
or oxtail. The food ration of lactating ?? is 
increased according to demand. 
REPRODUCTIVE  BEHAVIOUR 
Crab-eating foxes become sexually mature during 
the first year. The appearance of raised-leg 
urinations, which are common to both sexes, 
indicates the onset of sexual maturity. The cJ6\ 
like other canids, raise the hind leg back 
and outwards. Females raise the hind leg 
forward and rotate the rump slightly towards 
the marking site. Young c?<? begin scent- 
marking (using the raised-leg posture) at 
five months of age, but only one c? in each litter 
does so. This was observed regardless of whether 
the father was present or absent during the 
rearing and it is possible that the young <? which 
first establishes the behaviour might inhibit it in 
other (J siblings. Females have not been observed 
to develop the raised-leg posture until eight 
months of age. This sexual dimorphism might be 
due to an inhibitory influence of the mother on 
her daughters or might be a physiological differ- 
ence similar to that described for Red foxes 
Vulpes vulpes (Storm et al., 1976). 
Two $ siblings, captured as pups, came into 
oestrus at an estimated age of nine months and 
BREEDING 131 
DATE OF LAST 
LITTER OBSERVED DATE OF GESTATION LITTER NO. 
NO.       ? COPULATION PARTURITION PERIOD SIZE REARED COMMENTS 
I            I 8 Jan 1976 8 Mar 1976 59 2.1 2.1 ?x 9 months old when mated 
2 6 Jan 1976 
3 9 Jan 1976 
2           2 ? 25 Jun 1976 ? 2.2 2.2 
3        1 25 Aug 1976 23 Oct 1976 59 1-4 O.3 one ? hand-reared from day 
30 on 
4        3 2 Dec 1976 23 Jan 1977 52 5-1 5.1 sired by 3 from litter 1 
5         2 1 Jan 1977 24 Feb 1977 54 ? killed at birth (possibly by 
young of previous litter (2)) 
Table 1. Data on three breeding $ Crab-eating foxes Cerdocyon thous at the National Zoological Park, 
Washington. 
one ($x Table 1) became pregnant and success- 
fully reared her young. However, young ?? 
left with the family did not show a noticeable 
oestrous period at nine months. Young 33 are 
capable of breeding in the first year. A captive- 
born 6* (from the first litter) sired a litter (4) at 
nine months, and six-month-old 33 showed 
interest and attempted to mount their mother 
when she came into oestrus. 
The animals in the study group bred twice a 
year with approximately an eight month inter- 
birth interval (Table 1). Two oestrous periods in 
one year is a rare, but not unique, condition in 
wild canids (Kleiman, 1968; van Lawick & van 
Lawick-Goodall, 1971; Kleiman & Brady, 1978). 
In Venezuela, pregnant foxes have been found 
during most seasons (E. Mondolfi, pers. comm.), 
although on the llanos, young appear mainly in 
February and March (J. Eisenberg, pers. comm.). 
Copulatory behaviour in the Crab-eating fox 
was similar to that described for other canids 
(Kleiman, 1968; Ewer, 1973). Copulations were 
observed over a three-day period. Copulatory 
ties lasted from five to eight minutes and the 
pair stood back to back while tied. The average 
gestation period, calculated from the last 
observed copulation, was 56 days but there was 
considerable variation (Table 1). 
PARENTAL BEHAVIOUR 
Pregnant ?? remained close to the den as partur- 
ition approached. The 33 remained with their 
mates at birth without conflict. However, one $ 
whose pair-mate was removed before parturition 
reared the litter alone (litter i). Females did not 
attempt to exclude their mates from the den at 
birth and 33 generally slept in front of the nest- 
box. They frequently poked the muzzle into the 
nestbox and sniffed the ? and pups. If the pups 
were handled and a foreign scent was present, the 
3 would enter the box and sniff each pup. Both 
parents growled and barked at keepers who 
entered the outside yard during the early rearing 
period. 
For the first three days after parturition ?$ 
generally left the den either to eat or eliminate 
although several did not take food for the first 
two or three days. The mothers spent most of the 
time sleeping or licking the pups; however, they 
all left the nestbox for an occasional walk around 
the den. 
When returning to the nestbox or when 
changing position in the box, the $ avoided 
reclining directly on the pups. She would usually 
circle several times and reposition the pups by 
pushing with the muzzle, before lowering the 
head and shoulders to the ground and then 
gently sliding forward to lower the hind- 
quarters last. This usually resulted in the pups 
being positioned on the mother's ventral side. 
Occasionally pups would be dragged out of the 
nestbox because they held on to the teats as the ? 
left the box. They were retrieved from the den 
floor by either parent when they whined. Both 
parents also licked the pups' anogenital region 
and ingested the excreta. The 3 rarely entered the 
box to clean the pups but began cleaning them 
regularly around day 17 when they began to 
crawl out of the box. The parent would push the 
muzzle under the pup's belly and flip it on to its 
back so that the entire ventral area could be 
licked. As the pups grew older they attempted 
132 BREEDING 
to avoid die cleaning routine but the parents 
would chase, pin them with a foreleg and clean 
them. This behaviour decreased in frequency as 
the young foxes became efficient at escaping the 
adult's hold. 
During the early stages of rearing the adults 
were fed in the outdoor yards. The <J<J were not 
observed carrying food to the 99 but both 
parents were first seen transporting food to the 
young on day 16. Chunks of food were carried 
and dropped in the den rather than regurgitated. 
Adult 99 cache food randomly throughout the 
yards using the muzzle to cover it with soil in a 
typical canid fashion. 
A striking change in the 9$'s scent-marking 
behaviour occurred after the birth. They no 
longer marked the yards with raised-leg uri- 
nations nor were they observed to anal rub or 
rub the flanks against their mates' marks, all of 
which were commonly observed outside the 
rearing season. Neither did they cover the c?cj's 
marks during this period, although pairs of foxes 
generally mark die same spot in sequence 
(Kleiman & Brady, 1978). Scent-marking was 
resumed at c. 45 days after parturition and it is 
possible diat the cessation of scent-marking might 
function to minimise attraction of predators to the 
whelping site. 
DEVELOPMENT  OF PUPS 
Crab-eating fox pups are born with the eyes and 
ears closed and without teeth. They weigh 
between 120-160 g and gain weight rapidly 
(Fig. 1). The natal coat is charcoal grey with a 
buff patch in the inguinal region. The first 
changes occur on day 14 when the eyes and ears 
open and the canine teeth begin to erupt. At this 
time the buff inner ear pinnae also become visible. 
The pelage begins to change colour around day 
20 when the hair around the ears and eyes 
becomes grey. By day 25 the head is grey with a 
black muzzle and distinct black marks on the 
cheeks. The buff undercoat now extends from 
the chin to the anal region and down the inside 
of the flanks. By day 35 the entire coat is a 
lighter grey except for the paws, muzzle and tail 
which remain dark. The adult pelage is attained 
by day 45. 
Body measurements and tooth eruption dates 
were recorded for three litters and are presented in 
Tables 2 and 3. The Crab-eating fox is similar to 
Fig. 1. Growth rates of three litters of Crab-eating 
foxes Cerdocyon thous reared by their mothers. 
Black circle=2.i; triangle=2.2; open circle=0.3 
(1 removed for hand-rearing day 30). In each case, 
the symbol represents the mean litter weight 
while the vertical lines indicate the range in 
weights. 
other canids (Ewer, 1973) in that it lacks upper 
and lower premolar 1 in its milk dentition and 
that the carnassials are the first cheek teeth to 
erupt. Although regular oral examination was 
discontinued on day 50, subsequent checks 
revealed that the foxes began to lose their milk 
teeth at about five months of age. 
The development of the young may be 
divided into three periods (Ewer, 1973). The 
first is the early nesting stage when the young are 
completely dependent on the mother's milk for 
nutrition. In Crab-eating foxes this would 
correspond to the first 30 days after birth. The 
second period, a time of mixed nutritional 
dependency, lasts from day 30 to day 90 when 
the pups are completely weaned. Finally, there is 
a period of post-weaning dependency which lasts 
from day 90 to c. five months. In captivity the 
family unit may be extended beyond this date 
but in the wild is probably disbanded around this 
time. 
Pup health was generally good. However, two 
of the five pups from litter 3 died on day 5 from 
meningitis. Another pup from the same litter was 
M BREEDING 133 
LITTER I (2.1) LITTER 2 (2.2) LITTER 3 (0.3) 
TOTAL TAIL GIRTH NECK EARS  TOTAL TAIL GIRTH NECK EARS TOTAL TAIL GIRTH NECK EARS 
DAY LENGTH LENGTH LENGTH LENGTH LENGTH LENGTH 
I 22 6 II 8 closed 22 6 IO 8 closed 
7 27 8 12 10 closed 23 6 12 9 closed 
H 30 8 14 11 2 30 8 15 12 2 
21 40 13 20 16 32 9 15 13 2 32 ? I? 13 3 
28 42 15 23 17 38 11 20 14 4 35 ? 19 13 4 
35 49 16 24 18 44 13 22 15 4 41 ? 21 14 4 
42 54 18 25 19 47 14 23 15 4 47 22 15 5 
49 63 21 27 19 49 15 23 15 5 50 24 16 5 
56 64 21 30 19 56 16 25 16 5 52 24 16 5 
63 67 22 30 20 58 17 25 16 6 58 26 17 6 
70 71 22 30 20 64 20 28 18 6 
77 73 24 30 22 68 21 28 18 6 64 28 18 6 
84 76 24 31 22 70 22 29 19 6 
91 ? ? 73 23 31 20 6 66 30 18 6 
105 
?   77 23 31 20 6 73 32 20 6 
Table 2. Body measurements (in cm) of the first three litters shown on Table I. The figures given are the 
average for each litter. One of the pups in litter 3 was hand-reared from day 30 after being removed for 
veterinary treatment. 
UPPER JAW (days) LOWER JAW (days) 
?l 22-26 h 20-26 
la 20-23 h 20-23 
% 17-23 H 18-23 
c 14-16 c 14-16 
pirn pnii 
pm2 pniij 28-32 
pm8 30-35 pm3 27-30 
pm4 20-25 pm4 25-28 
mi nil 
ma ma 
ms 
Table 3. The range in days of tooth eruption in the 
three litters of ten pups shown in Tables 1 and 2. 
Oral examination was discontinued after day 50. 
born with splayed front and rear limbs. Although 
the pup moved with swimmerlike motions, it 
did not have difficulty in nursing. On day 30 
it was removed and the limbs were taped to- 
gether in the proper position by the veterinarian. 
After four days' restriction, the pup moved with 
a normal gait. Subsequent trial reintroductions 
to litter mates failed and it was hand-reared and 
later weaned on the feline diet. 
PUP    BEHAVIOUR 
Suckling touts were the pups' only major 
activity for the first two weeks of life. They were 
able to crawl but generally remained in contact 
with the mother. When she left the den, the pups 
moved into a pile, a behaviour which aids heat 
conservation and is observed in other canid 
species (Rheingold, 1963). As they grew older 
they constantly attempted to climb on top of each 
other which resulted in a period of scrambling 
and readjusting each time the pile was formed. 
The first observed interactions between litter 
mates occurred on day 13 during one of these 
periods. The pups mouthed each other's heads 
and attempted to stand on one another's backs. 
This mouthing later developed into biting to the 
muzzle, ears, cheeks and occasionally a limb or 
the tail. Muzzle wrestling and grappling appeared 
on day 17 and coincided with the development 
of walking. Both parents ignored these pup 
interactions. 
The pups suckled at frequent intervals for the 
first 50 days, although they were first observed to 
take solid food on day 20. They left the den for 
various periods beginning on day 28, but did not 
venture outside regularly until day 45. De- 
faecation outside the den entrance was first 
observed on day 35. 
The pups were efficient at begging and were 
able to extract even the choicest food item from 
their parents. With ears flattened laterally and 
tails wagging, they would crouch low to the 
in  NZ.P   hbroury 
134 BREEDING 
ground and approach the adult from the side. 
Although the parent usually fled, the pups, still in 
the begging posture, chased and nudged the 
corner of its mouth until the food was dropped. 
The same posture was used when attempting to 
suckle after day 50. As the pups grew older, the 
parents, especially the $, would punish them 
when they begged by grasping the pup's muzzle 
in the mouth and pinning it to the ground. The 
pup would whine, roll on its back and continue 
wagging its tail; a posture referred to as active 
submission (Schenkel, 1967). 
Family units were left together until serious 
fights occurred. In one family (litter 1) where the 
adult 6* was removed, serious fighting between 
two 6*0* occurred when they were five months 
old. This coincided with the onset of raised-leg 
urinations by one of the pups, although the 
adult $ might have been in oestrus. In other litters, 
where the adult 6* was present, no fighting 
occurred. 
In another family group (litter 2) the adult $ 
came into oestrus and copulated solely with the 
adult 6*. Both 6* juveniles showed interest and one 
son who used the raised-leg urination posture 
attempted to mount. The $ repelled him on all 
occasions. In this instance, the juveniles were left 
with the adult pair in order to observe whether 
they would assist the parents in rearing the new 
litter. The remains of the new litter were dis- 
covered on the morning of birth and it appeared 
that the juveniles had killed them. 
ACKNOWLEDGEMENTS 
I am grateful to D. Kleiman, J. Eisenberg, C. Wemmer 
and G. Svendsen for their advice throughout this pro- 
ject; to M. Ditton for her assistance in data collection 
and M. Hartman for typing the manuscript. This 
research was supported by a Smithsonian Research 
Foundation Grant to D. Kleiman and J. Eisenberg. 
PRODUCT MENTIONED IN THE TEXT 
Nebraska Brand Feline Food: manufactured by 
Central Nebraska Packing Co., North Platte, Nebraska 
69101, USA. 
REFERENCES 
COIMBRA FILHO, A. F. (1966): Notes on the reproduction 
and diet of Azara's fox Cerdocyon thous azarae and the 
hoary fox Duskyon vetulus at the Rio de Janeiro Zoo. 
Int. Zoo Yb. 6: 168-169. 
EWER, R. F. (1973): The carnivores. Ithaca, NY: Cornell 
University Press. 
KLEIMAN, D. G. (1968): Reproduction in the Canidae. 
Int. Zoo Yb. 8: 3-8. 
KLEIMAN, D. G. & BRADY, c. A. (1978): Coyote behavior 
in the context of recent canid research: problems and 
perspectives. In Coyote biology. Bekoff, M. (ed.). New 
York: Academic Press. 
RHEINGOLD, H. (1963): Maternal behavior in the dog. In 
Maternal behavior in mammals. Rheingold, H. (ed.). New 
York: John Wiley and Sons. 
SCHENKEL,  R.   (1967):   Submission:  its  features  and 
functions in the wolf and dog. Am. Zool. 7: 319-329. 
STORM, G., ANDREWS, R., PHILLIPS, R., BISHOP, A., SINIFF, 
D. & TESTER, J. (1976): Morphology, reproduction and 
mortality of midwestern red fox populations. Wildl. 
Monogr. 49: 1-82. 
VAN LA WICK,   H.    &  VAN  LAWICK-GOODALL,   J.   (1971): 
Innocent killers. Boston: Houghton Mifflin. 
Manuscript submitted 4 April 1977 
Printed in Great Britain by Henry Ling Ltd., at the Dorset Press, Dorchester, Dorset